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Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative.

ABSTRACT: Tomato breeding has been tremendously efficient in increasing fruit quality and quantity but did not focus on improving herbivore resistance. The biosynthetic pathway for the production of 7-epizingiberene in a wild tomato was introduced into a cultivated greenhouse variety with the aim to obtain herbivore resistance. 7-Epizingiberene is a specific sesquiterpene with toxic and repellent properties that is produced and stored in glandular trichomes. We identified 7-epizingiberene synthase (ShZIS) that belongs to a new class of sesquiterpene synthases, exclusively using Z-Z-farnesyl-diphosphate (zFPP) in plastids, probably arisen through neo-functionalization of a common ancestor. Expression of the ShZIS and zFPP synthases in the glandular trichomes of cultivated tomato resulted in the production of 7-epizingiberene. These tomatoes gained resistance to several herbivores that are pests of tomato. Hence, introduction of this sesquiterpene biosynthetic pathway into cultivated tomatoes resulted in improved herbivore resistance.

SUBMITTER: Bleeker PM

PROVIDER: S-EPMC3523864 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative.

Bleeker Petra M PM Mirabella Rossana R Diergaarde Paul J PJ VanDoorn Arjen A Tissier Alain A Kant Merijn R MR Prins Marcel M de Vos Martin M Haring Michel A MA Schuurink Robert C RC

Proceedings of the National Academy of Sciences of the United States of America 20121119 49

Tomato breeding has been tremendously efficient in increasing fruit quality and quantity but did not focus on improving herbivore resistance. The biosynthetic pathway for the production of 7-epizingiberene in a wild tomato was introduced into a cultivated greenhouse variety with the aim to obtain herbivore resistance. 7-Epizingiberene is a specific sesquiterpene with toxic and repellent properties that is produced and stored in glandular trichomes. We identified 7-epizingiberene synthase (ShZIS) ...[more]

PMID: 23169639

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Project description:Background and aimsStereochemical variation is widely known to influence the bioactivity of compounds in the context of pharmacology and pesticide science, but our understanding of its importance in mediating plant-herbivore interactions is limited, particularly in field settings. Similarly, sesquiterpene lactones are a broadly distributed class of putative defensive compounds, but little is known about their activities in the field.MethodsNatural variation in sesquiterpene lactones of the common cocklebur, Xanthium strumarium (Asteraceae), was used in conjunction with a series of common garden experiments to examine relationships between stereochemical variation, herbivore damage and plant fitness.Key resultsThe stereochemistry of sesquiterpene lactone ring junctions helped to explain variation in plant herbivore resistance. Plants producing cis-fused sesquiterpene lactones experienced significantly higher damage than plants producing trans-fused sesquiterpene lactones. Experiments manipulating herbivore damage above and below ambient levels found that herbivore damage was negatively correlated with plant fitness. This pattern translated into significant fitness differences between chemotypes under ambient levels of herbivore attack, but not when attack was experimentally reduced via pesticide.ConclusionsTo our knowledge, this work represents only the second study to examine sesquiterpene lactones as defensive compounds in the field, the first to document herbivore-mediated natural selection on sesquiterpene lactone variation and the first to investigate the ecological significance of the stereochemistry of the lactone ring junction. The results indicate that subtle differences in stereochemistry may be a major determinant of the protective role of secondary metabolites and thus of plant fitness. As stereochemical variation is widespread in many groups of secondary metabolites, these findings suggest the possibility of dynamic evolutionary histories within the Asteraceae and other plant families showing extensive stereochemical variation.

Project description:Background. Studies of ancestry are difficult in the tomato because it crosses with many wild relatives and species in the tomato clade that have diverged very recently. As a result, the phylogeny in relation to its closest relatives remains uncertain. By using the coding sequence from Solanum lycopersicum, S. galapagense, S. pimpinellifolium, S. corneliomuelleri, and S. tuberosum and the genomic sequence from S. lycopersicum 'Heinz', an heirloom line, S. lycopersicum 'Yellow Pear', and two of cultivated tomato's closest relatives, S. galapagense and S. pimpinellifolium, we have aimed to resolve the phylogenies of these closely related species as well as identify phylogenetic discordance in the reference cultivated tomato. Results. Divergence date estimates suggest that the divergence of S. lycopersicum, S. galapagense, and S. pimpinellifolium happened less than 0.5 MYA. Phylogenies based on 8,857 coding sequences support grouping of S. lycopersicum and S. galapagense, although two secondary trees are also highly represented. A total of 25 genes in our analysis had sites with evidence of positive selection along the S. lycopersicum lineage. Whole genome phylogenies showed that while incongruence is prevalent in genomic comparisons between these genotypes, likely as a result of introgression and incomplete lineage sorting, a primary phylogenetic history was strongly supported. Conclusions. Based on analysis of these genotypes, S. galapagense appears to be closely related to S. lycopersicum, suggesting they had a common ancestor prior to the arrival of an S. galapagense ancestor to the Galápagos Islands, but after divergence of the sequenced S. pimpinellifolium. Genes showing selection along the S. lycopersicum lineage may be important in domestication or selection occurring post-domestication. Further analysis of intraspecific data in these species will help to establish the evolutionary history of cultivated tomato. The use of an heirloom line is helpful in deducing true phylogenetic information of S. lycopersicum and identifying regions of introgression from wild species.

Project description:BACKGROUND: Cultivated grapevines, Vitis vinifera subsp. sativa, evolved from their wild relative, V. vinifera subsp. sylvestris. They were domesticated in Central Asia in the absence of the powdery mildew fungus, Erysiphe necator, which is thought to have originated in North America. However, powdery mildew resistance has previously been discovered in two Central Asian cultivars and in Chinese Vitis species. RESULTS: A set of 380 unique genotypes were evaluated with data generated from 34 simple sequence repeat (SSR) markers. The set included 306 V. vinifera cultivars, 40 accessions of V. vinifera subsp. sylvestris, and 34 accessions of Vitis species from northern Pakistan, Afghanistan and China. Based on the presence of four SSR alleles previously identified as linked to the powdery mildew resistance locus, Ren1, 10 new mildew resistant genotypes were identified in the test set: eight were V. vinifera cultivars and two were V. vinifera subsp. sylvestris based on flower and seed morphology. Sequence comparison of a 620 bp region that includes the Ren1-linked allele (143 bp) of the co-segregating SSR marker SC8-0071-014, revealed that the ten newly identified genotypes have sequences that are essentially identical to the previously identified mildew resistant V. vinifera cultivars: 'Kishmish vatkana' and 'Karadzhandal'. Kinship analysis determined that three of the newly identified powdery mildew resistant accessions had a relationship with 'Kishmish vatkana' and 'Karadzhandal', and that six were not related to any other accession in this study set. Clustering procedures assigned accessions into three groups: 1) Chinese species; 2) a mixed group of cultivated and wild V. vinifera; and 3) table grape cultivars, including nine of the powdery mildew resistant accessions. Gene flow was detected among the groups. CONCLUSIONS: This study provides evidence that powdery mildew resistance is present in V. vinifera subsp. sylvestris, the dioecious wild progenitor of the cultivated grape. Four first-degree parent progeny relationships were discovered among the hermaphroditic powdery mildew resistant cultivars, supporting the existence of intentional grape breeding efforts. Although several Chinese grape species are resistant to powdery mildew, no direct genetic link to the resistance found in V. vinifera could be established.

Dataset Information

Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative.

Publications

Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative.

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